Вы находитесь на странице: 1из 8

6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

Effectsofglucoseonthebrain
Creators:ShamikMukherji,AlanJacobson
Thoughthereisagreatamountofattentiongiventotheeffectsofdiabetesontheperipheralnervoussystem,itisimportant
nottooverlookthediseaseseffectsonourbrains.Whileotherorgansinthebodymayrelyonalternativesourcesofenergy,
suchasfattyacids,thebrainreliesalmostsolelyonglucose,usingketonesasalastresort.Forthisreason,thebloodbrain
barrierisrichinGlut1activeglucosetransporters,andover99%oftheglucosethatpassesitisusedbyneuronsandglia.
Thus,themetabolicefficiencyandcontinuousdemandsofthebrainrenderituniquelysusceptibletofluctuationsinglucose
concentrationinthebody.

Aswediscussinthischapter,hyperglycemiaandhypoglycemiabothcanhavedetrimentaleffectsoncognitionaswellas
mood.TheseeffectsareevidentinpeoplewithType1andType2diabetes.Themostcommonmanifestationsofcognitive
deficitareneuralslowing,attentiondeficit,andexecutivefunctioning.Patientswithtype2diabetesinparticulardomorepoorly

inmeasuresoflearningandmemory[1].

Itisimportanttonotethatinahospitalsettingpatientswithoutdiabetescanbecomehyperglycemic,andthesepatientshave

anincreasedmortalityrisk[2].Stressinducedhyperglycemiainpatientswithoutdiabetescanoccurduringperiodsofacute

illnessandmaybeduetohormonalcascades,particularlyincreasesinepinephrine,cortisol,growthhormoneandglucagon[3].
Patientsmayhaveprediabetes,ormayhavefrankdiabetesthatisundiagnosed.Amonghyperglycemicpatientsingeneral
medicinewards,onestudyfoundthat12%wereundiagnosed,andthattheyhad18.3timesthemortalityrateoftheir
normoglycemicpeers.Thesepatientsalsohadlongerhospitalstays,wereadmittedtotheICUmoreoften,andlargelyhad

theirhyperglycemiauntreatedthroughoutthecourseoftheirstay[4].Similarly,inpatientsbothwithandwithoutdiabetes,

hypoglycemiaisassociatedwithincreasedinpatientmortalityandincreasedhospitallengthofstay[5][6].

Aclinicalawarenessofapatientsglycemicstate,especiallyifthepersonhasdiabetes,iskeytoprotectinghigherneurological
functioning,suchasmoodandcognition,aswellasmitigatingtheriskofmortality.Inthischapter,wewillfurtherdiscussthe
acuteandchroniceffectsofbothhypoglycemiaandhyperglycemiaonthebrain.

AcuteHyperglycemia
Theeffectsofacutehyperglycemiaonmoodandcognitioninpeoplewithdiabetesarecontroversial.Onestudyshowedthat
peoplewithtype2diabetesmaynotexhibitchangesincognitionormoodinshortperiodsofmildhyperglycemia.Interestingly,

patientsmayreportfeelingsofwellbeingandlessangerduringperiodsofbriefmildhyperglycemia[7].Otherresearch
contradictsthis,reportingincreasedirritabilityanddecreasedfeelingsofwellbeinginpeoplewithtype1andtype2diabetes

whoareacutelyhyperglycemic[8][9].Itappearsthatglucoselevelandnotvariabilityisthedeterminantofmoodvariation[9].
Patientswithlowerpostprandialglucose,however,dobetterthanthosewithhigherpostprandialglucoseincognitivetesting
[10].

http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 1/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

Inpragmaticstudiesinvolvingpeoplewithdiabeteswhosedrivingabilitiesareassessed,acutehyperglycemiacanleadto

tirednessanddecreasedvisualacuity.Thiscanthencauseincorrecttreatmentadjustmentprecipitatinghypoglycemia[11].
Peoplewithtype1diabeteshavebeenshowntohavelowerverbalandoverallIQscoresduringperiodsofacute
hyperglycemia[12].BothpeoplewithType1andType2diabeteshaveexhibitedlowercognitivescoreswhenbloodglucose

increasespast15mmol/l[13].Thus,acutehyperglycemiaappearstohavedetrimentaleffectsthatmayperturbdaytoday
functionsofbothpeoplewithType1andType2diabetes.

ChronicHyperglycemia
Theeffectsofchronichyperglycemiaaremorepronouncedthanthoseofacutehyperglycemia.Longtermhyperglycemiaas
seeninpeoplewithdiabetesappearstoresultinsignificantchangesintheirmoodandcognitivestate.Forinstance,type2

diabetesisbidirectionallyassociatedwithdepression[14].Indeed,peoplewithtype2diabeteswhohaveahemoglobinHbA1c

withinthenormalnondiabeticrangeexhibitfewersymptomsofdepressionthanthosewithhighHbA1c[15].

Peoplewithtype1diabetesperformsignificantlyworsethantheirnondiabeticpeersinattention,psychomotorefficiency,

cognitiveflexibility,andgeneralintelligence[16].Theetiologyoftheseeffectsisunclear,andisthesourceofmuchresearch.
StudieshavefoundthathighHbA1clevelspredictcognitivedeficitanditsdevelopmentovertimeinpatientswithandwithout

diabetes[17].Hyperglycemiaandadiposityareassociatedwithpoorcognitivefunctioninginmiddleagedpeoplewithout
diabetesaswell,whichshowsthatthesefactorsindependentlyaffectcognitivefunctioningoutsideoftheusualcomplications

ofdiabetes[18].Childrenwithtype1diabetesmayhavepoorerworkingmemoryasaresultofhyperglycemia.Childrenwith
multipleriskfactors,ofwhichhyperglycemiawasone,appearedtodoworseintestsofverbalabilities,workingmemory,and
mentalefficiency.Childrenwithotherriskfactors,suchasearlieronsetdiabetesandhypoglycemia,inconjunctionwith
hyperglycemia,didworsethanpeersinthesametests.Chronichyperglycemiaincreasestheriskofcognitivedeclineinthose
withdiabetesby60100%.ThisisprimarilyduetoahigherriskofvasculardementiaratherthanthatofAlzheimersdisease
[19].TheriskofAlzheimersdiseaseinpeoplewithdiabetes,however,iselevatedaswell[20].Thereisa50100%increased

riskofstrokeinpeoplewithdiabetesversusanormalpopulation,withastrokerelativeriskof1.15(95%CI1.081.23)for

every1%(11mmol/mol)riseinHbA1c[21].Theetiologyofthisisunderstudy.Endocrineabnormalities,suchaschangesin
insulinandamyloidmetabolism,andincreasedoxidativestressmaybeatfault.Inflammatoryphenomena,evidencedbyan

increaseinCRP,IL6,andTNfconcentration,havebeenstudiedinrelationtothisphenomenonaswell[22].

ArterialspinlabelingMRIstudieshaveshownthatcerebralbloodflowispoorerinpeoplewithdiabetes,andthatthesepeople

exhibitsignsofcorticalandsubcorticalatrophy[23].Lacunarinfarctsoccurmorefrequentlyinpeoplewithdiabetes,andthereis

asignificantassociationbetweencognitivedysfunction,lacunarinfarcts,andtheirprevalenceindiabetes[24].Hippocampal
atrophymaybeanothercauseofcognitivedysfunction,asitsdegreeispredictedbyHbA1c.A1015%lossinhippocampal

volumehasbeendocumentedintheelderlywithprediabetes,andisassociatedwithmemoryimpairments[25].The
hippocampusishighlyvulnerabletohypoglycemicdamage,aswouldbeexpectedinpeoplewithType1diabetes,however,
studiesshowthatcorticalatrophyinthehippocampusismorepronouncedinthosewithType2diabetes.Thismaybebecause

peoplewithType2diabetesareolderonaveragethanpeoplewithType1diabetes[26][27].Thereasonsfortheincreasedrisk
ofdementiaand/orcognitivedeficitinthosewithdiabetesmayultimatelybemultifactorial.

AcuteHypoglycemia
Despitetheconflictingevidenceregardingtheeffectsofrecurrentepisodesofhypoglycemiaonthebrain,itisgenerally

acceptedthathypoglycemiacausesneuronalinjuryandimpairmentsinmoodandcognition[28][29].Moderateepisodesof

http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 2/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

hypoglycemiahavebeenshowntocauseshorttermcognitivedeficits,whichincreasetheriskofmotorvehicleaccidents[29].
InavehicledrivingstudyonpeoplewithType1diabetes,cognitionwasshowntoreturntobaselineuponreturntoeuglycemia
[30].Thelengthoftimeittakesforonetorecovercognitivelyfromhypoglycemicepisodeisamatterofdebateandmaybe

relatedtotheseverityofthehypoglycemia.Cognitiverecoverymaytakeseveraldaysinthosewhohaveexperiencedsevere

hypoglycemia[31][32].Inhealthypeoplewithoutdiabetes,acuteepisodesofhypoglycemiacausefeelingsoftirednessand

increasedtension[33].InpeoplewithType1diabetes,acutehypoglycemiacausesdeficitsincognitivetaskcompletion,

increasedanxiety,anddecreasedenergy[34].

Thereisevidencethatanextendedepisodeofseverehypoglycemiacausesdirectneuronalnecrosis[35].Thebrains
metabolismitselfchangesafterrepeatedepisodesofhypoglycemiainashortamountoftime.Hypoglycemicepisodeswithin

1224hofeachotherresultinasuppressionofcounterregulatoryresponsestosubsequenthypoglycemicepisodes[36].Asthis
isfoundinbothtype1andtype2diabetes,itmayalsobeanadaptivemechanismbywhichthebrainbetterresistsfurther

hypoglycemicinsult,andmaybeexpressedevenatthecellularlevel[37][38][39].However,thisincreasesthepatientsriskof
subsequenthypoglycemia.Thepatientsawarenessoftheirownsymptoms,asaresultofthesemechanisms,becomes

impaired[39][40].Poorhypoglycemiaawarenessinpeoplewithdiabetescanbedangerousbecauseaffectedindividualsdonot
realizethattheirbloodglucoseislow,andextremeanduncorrectedhypoglycemiamayleadtounconsciousnessandeven
death.

Inpeoplewithtype1diabetes,pulsedarterialspinlabelingandBOLDfMRIstudieshavedemonstratedincreasedbloodflowin
severalbrainregionssuchasthehypothalamus,brainstem,anteriorcingulatedcortex,uncus,andputamenduringperiodsof

mildhypoglycemia,whichmaysuggestthatthesestructuresareespeciallysensitivetoevensmallbloodglucosechanges[41]
[42].Thus,evensmallacuteglycemicchangesmaybeofclinicalimportance.

ExposuretoRecurrentHypoglycemia
Theeffectsofrecurrenthypoglycemiaoncognitionaresubjecttodebate.Multiplehypoglycemicepisodesmaybeexperienced
inthosewithtype1diabeteswhoundergointensiveinsulintherapy.Repeatedhypoglycemiainbothtype1andtype2diabetes
hasbeenshowntocauseimpairedhypoglycemiaawareness,andanalterationoftheglycemicthresholdsthatthebrainis

usedto[43].Asmentionedearlier,thispoorawarenessofhypoglycemiamayleadtopoortreatmentadjustmentpractices,
whichcouldthenleadtounconsciousnessordeathasthehypoglycemiabecomesmoresevere.

Analysisofthe18yearDCCTtrialshowednosignificantdeclineincognitioninpersonswithtype1diabetes,despitehigh

frequencyofhypoglycemiccomaand/orseizures[44].Theremay,however,beadaptivechangesthatunderliereducedcerebral
efficiencyinpeoplewithType1diabetes.PeoplewithType1diabeteshavebeenshowntohaveincreasedbrainactivationin
severalregions(bilateralfrontalandparietalcortices,insula,thalamus,andcerebellum)duringperiodsofhypoglycemia.Higher
HbA1cwasassociatedwithloweractivationintherightparahippocampalgyrusandamygdalaaswell,whichcouldindicate
compensatoryrecruitment.Thus,whilecognitivedifferencesmaynotbeevidentinthosewithahistoryofhypoglycemia,such
peoplemayrequireahigherlevelofbrainactivationtomaintainthesamelevelofcognitivefunctionastheirpeerswithout

diabetes[45].

Certainnegativeeffectsofrecurrenthypoglycemiahavebeenuncoveredusingneuroimagingtechniques.VoxelBased
Morphometry(VBM)studiessuggestthatahigherselfreportedfrequencyofseverehypoglycemiceventswereassociatedwith

graymatterdensitylosses,particularlyintheleftcerebrellarposteriorlobeandthelimbicunci[46].Thereisevidencethatthe
cerebellumisinvolvedinhigherexecutivefunctioning,language,andaffect.Insulttothisregionmayresponsibleforseveral
http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 3/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

cognitivedeficits[47].

Personswithtype2diabetesdonotundergorepeatedepisodesofhypoglycemiaasfrequentlyasthosewithtype1diabetes
[48].Thereissomedebateastotheeffectsofrecurrenthypoglycemiaonthedevelopmentofcognitivedysfunctionand

dementiainthosewithtype2diabetes.Studiesoffercontradictoryevidenceregardingtherelationshipbetweenhypoglycemic

episodesandlaterdementiadevelopment[49][50][51].Furtherresearchisneededtohelpelucidatethelongtermeffectsof
recurrenthypoglycemicepisodesoncognition,mood,anddementiadevelopment.

References
1.^McCrimmonRJ,RyanCM,FrierBM.Diabetesandcognitivedysfunction.Lancet.

2.^ConnerTM,FlesnerGurleyKR,BarnerJC.Hyperglycemiainthehospital

3.^LevetanCS,MageeMF.Hospitalmanagementofdiabetes.EndocrinolMe

4.^UmpierrezGE,IsaacsSD,BazarganN,YouX,ThalerLM,KitabchiAE.Hyperglycemia:anindependentmarkerofin
hospitalmortalityinpatientswithundiagnoseddiabetes.JClinEndocrinolMetab200287:97882.

5.^TanHK,FlanaganD.Theimpactofhypoglycaemiaonpatientsadmittedtohospitalwithmedicalemergencies.Diabet
Med.2013May30(5):57480.

6.^NirantharakumarK,MarshallT,KennedyA,NarendranP,HemmingK,ColemanJJ.Hypoglycaemiaisassociatedwith
increasedlengthofstayandmortalityinpeoplewithdiabeteswhoarehospitalized.DiabetMed.2012Dec29(12):e4458.

7.^PaisI,HallschmidM,JauchCharaK,SchmidSM,OltmannsKM,PetersA,BornJ,SchultesB.Moodandcognitive
functionsduringacuteeuglycaemiaandmildhyperglycaemiaintype2diabeticpatients.ExpClinEndocrinolDiabetes.
2007Jan115(1):426.

8.^SommerfieldAJ,DearyIJ,FrierBM.Acutehyperglycemiaaltersmoodstateandimpairscognitiveperformancein
peoplewithtype2diabetes.DiabetesCare.2004Oct27(10):233540.

9.^HermannsS,ScheffC,KulzerB,WeyersP,PauliP,KubiakT,HaakT.Assoicationofglucoselevelsandglucose
variabilitywithmoodintype1diabetespatients.Diabetologia.2007March50930933.

10.^PapanikolaouY,PalmerH,BinnsMA,JenkinsDJ,GreenwoodCE.Bettercognitiveperformancefollowingalow
glycaemicindexcomparedwithahighglycaemicindexcarbohydratemealinadultswithtype2diabetes.Diabetologia.
2006May49(5):85562.Epub2006Mar1

11.^SeegerR,LehmannR.[Drivingabilityandfitnesstodriveinpeoplewithdiabetesmellitus].TherUmsch.2011
May68(5):24952.

12.^NorthamEA,RankinsD,LinA,etal.Centralnervoussystemfunctioninyouthwithtype1diabetes12yearsafter
diseaseonset.DiabetesCare200932::445450.

13.^CoxDJ,KovatchevBP,GonderFrederickLAetal,etalRelationshipsbetweenhyperglycaemiaandcognitive
performanceamongadultswithtype1andtype2diabetes.DiabetesCare200528::7177.

14.^MezukB,EatonWW,AlbrechtS,GoldenSH.Depressionandtype2diabetesover

15.^RustadJK,MusselmanDL,NemeroffCB.Therelationshipofdepressionanddiabetes:pathophysiologicaland
http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 4/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

treatmentimplications.Psychoneuroendocrinology.2011Oct36(9):127686.

16.^BrandsAM,BiesselsGJ,deHaanEH,KappelleLJ,KesselsRP.Theeffectsof

17.^RavonaSpringerR,MoshierE,SchmeidlerJ,GodboldJ,AkrivosJ,RappM,GrossmanHT,WysockiM,Silverman
JM,HaroutunianV,BeeriMS.Changesinglycemiccontrolareassociatedwithchangesincognitioninnondiabetic
elderly.JAlzheimersDis.201230(2):299309.

18.^SanzCM,RuidavetsJB,BongardV,MarquiJC,HanaireH,FerriresJ,AndrieuS.RelationshipBetweenMarkersof
InsulinResistance,MarkersofAdiposity,HbA1c,andCognitiveFunctionsinaMiddleAgedPopulationBasedSample:
theMONALISAStudy.DiabetesCare.2013Jun36(6):151221.

19.^GreggEW,YaffeK,CauleyJA,RolkaDB,BlackwellTL,NarayanKM,CummingsSR.Isdiabetesassociatedwith
cognitiveimpairmentandcognitivedeclineamongolderwomen?StudyofOsteoporoticFracturesResearchGroup.Arch
InternMed.2000Jan24160(2):17480.PubMedPMID:106477

20.^FolsomAR,RasmussenML,ChamblessLE,HowardG,CooperLS,SchmidtMI,HeissG.Prospectiveassociationsof
fastinginsulin,bodyfatdistribution,anddiabeteswithriskofischemicstroke.TheAtherosclerosisRiskinCommunities

21.^SelvinE,BolenS,YehHC,WileyC,WilsonLM,MarinopoulosSS,FeldmanL,

22.^WhitmerRA.Type2diabetesandriskofcognitiveimpairmentanddementia.CurrNeurolNeurosciRep.2007
Sep7(5):37380.Review.

23.^LastD,AlsopDC,AbduljalilAM,MarquisRP,deBazelaireC,HuK,Cavallerano

24.^vanHartenB,deLeeuwFE,WeinsteinHC,ScheltensP,BiesselsGJ.Brainimaginginpatientswithdiabetes:a
systematicreview.DiabetesCare.2006Nov29(11):253948.Review.

25.^GoldSM,DziobekI,SweatV,TirsiA,RogersK,BruehlH,TsuiW,RichardsonS,JavierE,ConvitA.Hippocampal
damageandmemoryimpairmentsaspossibleearlybraincomplicationsoftype2diabetes.Diabetologia.2007
Apr50(4):7119.Epub2007Feb14.

26.^McCrimmonRJ,RyanCM,FrierBM.Diabetesandcognitivedysfunction.Lancet.

27.^AuerRN.Hypoglycemicbraindamage.MetabBrainDis200419:16975.

28.^CoxDJ,GonderFrederickLA,KovatchevBP,JulianDM,ClarkeWL.Progressivehypoglycemiasimpactondriving
simulationperformance:occurrence,awarenessandcorrection.DiabetesCare200023:16370.

29.^RyanC,GurtuncaN,BeckerD.Hypoglycemia:acomplicationofdiabetestherapyinchildren.PediatrClinNorthAm.
2005Dec52(6):170533.

30.^CampbellLK,GonderFrederickLA,BroshekDK,KovatchevBP,AndersonS,ClarkeWL,CoxDJ.Neurocognitive
DifferencesBetweenDriverswithType1DiabeteswithandwithoutaRecentHistoryofRecurrentDrivingMishaps.IntJ
DiabetesMellit.2010Aug12(2):7377

31.^StrachanMWJ,DearyIJ,EwingFME,FrierBM.Recoveryofcognitivefunctionandmoodafterseverehypoglycemiain
adultswithinsulintreateddiabetes.DiabetesCare.200023:305312

32.^ZammittNN,WarrenRE,DearyIJ,FrierBM.Delayedrecoveryofcognitivefunctionfollowinghypoglycemiainadults
http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 5/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

withtype1diabetes.Diabetes.200857:732736

33.^GoldAE,MacLeodKM,FrierBM,DearyIJ.Changesinmoodduringacutehypoglycemiainhealthyparticipants.JPers
SocPsychol.1995Mar68(3):498504.

34.^McAulayV,DearyIJ,SommerfieldAJ,MatthewsG,FrierBM.Effectsofacutehypoglycemiaonmotivationand
cognitiveinterferenceinpeoplewithtype1diabetes.JClinPsychopharmacol.2006Apr26(2):14351.

35.^AuerRN.Hypoglycemicbraindamage.MetabBrainDis200419:16975.

36.^HellerSR,CryerPE.Reducedneuroendocrineandsymptomaticresponsestosubsequenthypoglycemiaafter1
episodeofhypoglycemiainnondiabetichumans.Diabetes.1991Feb40(2):2236.

37.^GersteinHC,MillerME,ByingtonRP,GoffDCJr,BiggerJT,BuseJB,CushmanWC,GenuthS,IsmailBeigiF,Grimm
RHJr,ProbstfieldJL,SimonsMortonDG,FriedewaldWT.Effectsofintensiveglucoseloweringintype2diabetes.N
EnglJMed.2008Jun12358(24):254559.

38.^FanelliCG,EpifanoL,RambottiAM,PampanelliS,DiVincenzoA,ModarelliF,LeporeM,AnnibaleB,CiofettaM,
BottiniP,etal.Meticulouspreventionofhypoglycemianormalizestheglycemicthresholdsandmagnitudeofmostof

39.^McCrimmonRJ.UpdateintheCNSresponsetohypoglycemia.JClinEndocrinolMetab.2012Jan97(1):18.doi:
10.1210/jc.20111927.Review.

40.^CryerPE.BantingLecture.Hypoglycemia:thelimitingfactorinthemanagementofIDDM.Diabetes.1994
Nov43(11):137889.Review.

41.^PageKA,WilliamsonA,YuN,McNayEC,DzuiraJ,McCrimmonRJ,SherwinRS.Mediumchainfattyacidsimprove
cognitivefunctioninintensivelytreatedtype1diabeticpatientsandsupportinvitrosynaptictransmissionduringacute
hypoglycemia.Diabetes.2009May58(5):123744.

42.^McCrimmonRJ.UpdateintheCNSresponsetohypoglycemia.JClinEndocrinolMetab.2012Jan97(1):18.doi:
10.1210/jc.20111927.Review.

43.^McCrimmonRJ,RyanCM,FrierBM.Diabetesandcognitivedysfunction.Lancet.

44.^JacobsonAM,MusenG,RyanCM,SilversN,ClearyP,WaberskiB,BurwoodA,WeingerK,BaylessM,DahmsW,
HarthJ.Longtermeffectofdiabetesanditstreatmentoncognitivefunction.NEnglJMed.2007May3356(18):184252.
Erratumin:NEnglJMed.2009Nov5361(19):1914.

45.^BoloNR,MusenG,JacobsonAM,WeingerK,McCartneyRL,FloresV,RenshawPF,SimonsonDC.Brainactivation
duringworkingmemoryisalteredinpatientswithtype1diabetesduringhypoglycemia.Diabetes.2011Dec60(12):3256
64.

46.^MusenG,LyooIK,SparksCR,WeingerK,HwangJ,RyanCM,JimersonDC,HennenJ,RenshawPF,JacobsonAM.
Effectsoftype1diabetesongraymatterdensityasmeasuredbyvoxelbasedmorphometry.Diabetes.2006
Feb55(2):32633.

47.^SchmahmannJD,ShermanJC.Thecerebellarcognitiveaffectivesyndrome.Brain.1998Apr121(Pt4):56179.

48.^HellerSR,ChoudharyP,DaviesC,etal.Riskofhypoglycaemiaintypes1and2diabetes:Effectsoftreatment

http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 6/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

modalitiesandtheirduration.Diabetologia200750:11401147

49.^ReijmerYD,vandenBergE,RuisC,KappelleLJ,BiesselsGJ.Cognitivedysfunctioninpatientswithtype2diabetes.
DiabetesMetabResRev.2010Oct26(7):50719.

50.^WhitmerRA,KarterAJ,YaffeK,QuesenberryJ,SelbyJV.Hypoglycemicepisodesandriskofdementiainolder
patientswithtype2diabetesmellitus.JAmMedAssoc2009301:15651572.

51.^BruceDG,DavisWA,CaseyGP,etal.Severehypoglycaemiaandcognitiveimpairmentinolderpatientswithdiabetes:
TheFremantleDiabetesStudy.Diabetologia200952:18081815.

Comments
Nobodyhascommentedonthisarticle

CommentingisonlyavailableforregisteredDiapediausers.Pleaseloginorregisterfirst.

DOI
http://dx.doi.org/10.14496/dia.61047161570.6

Creators

ShamikMukherji

AlanJacobson

Sectioneditor

RichardHolt

Complexity
3Competent

Comments
Nobodyhascommentedonthisarticleyet.

Citationstyle
Pleaseusethefollowingformatwhenreferencingthisarticle:

Mukherji,Shamik,Jacobson,Alan.Effectsofglucoseonthebrain[internet].2014Aug13Diapedia61047161570rev.no.6.
Availablefrom:http://dx.doi.org/10.14496/dia.61047161570.6

Aboutthispage

http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 7/8
6/10/2016 EffectsofglucoseonthebrainAssociateddisordersDiapedia,TheLivingTextbookofDiabetes

Lastmodifiedon13August2014at01:56PM

http://www.diapedia.org/associateddisorders/61047161570/effectsofglucoseonthebrain 8/8

Вам также может понравиться